Genetic Modulation of c-di-GMP Turnover Affects Multiple Virulence Traits and Bacterial Virulence in Rice Pathogen Dickeya zeae.
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SUBMITTER: Chen Y
PROVIDER: S-EPMC5113947 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:The phytopathogen Dickeya zeae MS2 is a particularly virulent agent of banana soft rot disease. To begin to understand this banana disease and to understand the role of quorum sensing and quorum-sensing-related regulatory elements in D. zeae MS2, we sequenced its genome and queried the sequence for genes encoding LuxR homologs. We identified a canonical LuxR-LuxI homolog pair similar to those in other members of the genus Dickeya The quorum-sensing signal for this pair was N-3-oxo-hexanoyl-homoserine lactone, and the circuit affected motility, cell clumping, and production of the pigment indigoidine, but it did not affect infections of banana seedlings in our experiments. We also identified a luxR homolog linked to a gene annotated as encoding a proline iminopeptidase. Similar linked pairs have been associated with virulence in other plant pathogens. We show that mutants with deletions in the proline iminopeptidase gene are attenuated for virulence. Surprisingly, a mutant with a deletion in the gene encoding the LuxR homolog shows normal virulence.IMPORTANCE Dickeya zeae is an emerging banana soft rot pathogen in China. We used genome sequencing and annotation to create an inventory of potential virulence factors and virulence gene regulators encoded in Dickeya zeae MS2, a particularly virulent strain. We created mutations in several genes and tested these mutants in a banana seedling infection model. A strain with a mutated proline iminopeptidase gene, homologs of which are important for disease in the Xanthomonas species phytopathogens, was attenuated for soft rot symptoms in our model. Understanding how the proline iminopeptidase functions as a virulence factor may lead to insights about how to control the disease, and it is of general importance as homologs of the proline iminopeptidase occur in dozens of plant-associated bacteria.
| S-EPMC6856320 | biostudies-literature
Project description:Dickeya zeae is a phytopathogenic bacterium causing soft rot diseases in a wide range of economically important crops. Here we present the draft genome sequence of strain ZJU1202, which is the causal agent of rice foot rot in China. The draft genome will contribute to epidemiological and comparative genomic studies and the quarantine of this devastating phytopathogen.
| S-EPMC3416210 | biostudies-literature
Project description:Dickeya zeae is an important and aggressive bacterial phytopathogen that can cause substantial economic losses in banana and rice plantations. We previously showed that c-di-GMP signaling proteins (cyclases/phosphodiesterases) in D. zeae strain EC1 play a significant role in the bacterial sessile-to-motile transition. To determine whether there is any synergistic effect among these c-di-GMP signaling proteins, we prepared a series of mutant strains by generating consecutive in-frame deletions of the genes encoding diguanylate cyclases (which make c-di-GMP) and phosphodiesterases (which break down c-di-GMP), respectively, using EC1 as a parental strain. The results showed that the complete deletion of all the putative diguanylate cyclases resulted in significantly increased bacterial motility and abrogated biofilm formation but did not appear to affect pathogenicity and virulence factor production. In contrast, the deletion of all the c-di-GMP phosphodiesterase genes disabled motility and prevented the invasion of EC1 into rice seeds. By measuring the c-di-GMP concentrations and swimming motility of all the mutants, we propose that c-di-GMP controlled swimming behavior through a multitiered program in a c-di-GMP concentration-dependent manner, which could be described as an L-shaped regression curve. These features are quite different from those that have been shown for other bacterial species such as Salmonella and Caulobacter crescentus Further analysis identified three c-di-GMP signaling proteins, i.e., PDE10355, DGC14945, and PDE14950, that play dominant roles in influencing the global c-di-GMP pool of strain EC1. The findings from this study highlight the complexity and plasticity of c-di-GMP regulatory circuits in different bacterial species.IMPORTANCEDickeya zeae is the etiological agent of bacterial foot rot disease, which can cause massive economic losses in banana and rice plantations. Genome sequence analysis showed that D. zeae strain EC1 contains multiple c-di-GMP turnover genes, but their roles and regulatory mechanisms in bacterial physiology and virulence remain vague. By generating consecutive in-frame deletion mutants of the genes encoding c-di-GMP biosynthesis and degradation, respectively, we analyzed the individual and collective impacts of these c-di-GMP metabolic genes on the c-di-GMP global pool, bacterial physiology, and virulence. The significance of our study is in identifying the mechanism of c-di-GMP signaling in strain EC1 more clearly, which expands the c-di-GMP regulating patterns in Gram-negative species. The methods and experimental designs in this research will provide a valuable reference for the exploration of the complex c-di-GMP regulation mechanisms in other bacteria.
| S-EPMC7733949 | biostudies-literature
Project description:Studies on bacterial plant diseases have thus far been focused on the single bacterial species causing the disease, with very little attention given to the many other microorganisms present in the microbiome. This study intends to use pathobiome analysis of the rice foot rot disease, caused by Dickeya zeae, as a case study to investigate the effects of this bacterial pathogen to the total resident microbiome and to highlight possible interactions between the pathogen and the members of the community involved in the disease process. The microbiome of asymptomatic and the pathobiome of foot-rot symptomatic field-grown rice plants over two growing periods and belonging to two rice cultivars were determined via 16S rRNA gene amplicon sequencing. Results showed that the presence of D. zeae is associated with an alteration of the resident bacterial community in terms of species composition, abundance and richness, leading to the formation of microbial consortia linked to the disease state. Several bacterial species were significantly co-presented with the pathogen in the two growing periods suggesting that they could be involved in the disease process. Besides, culture-dependent isolation and in planta inoculation studies of a bacterial member of the pathobiome, identified as positive correlated with the pathogen in our in silico analysis, indicated that it benefits from the presence of D. zeae. A similar microbiome/pathobiome experiment was also performed in a symptomatically different rice disease evidencing that not all plant diseases have the same consequence/relationship with the plant microbiome. This study moves away from a pathogen-focused stance and goes towards a more ecological perception considering the effect of the entire microbial community which could be involved in the pathogenesis, persistence, transmission and evolution of plant pathogens.
| S-EPMC9292192 | biostudies-literature
Project description:BackgroundDickeya zeae is the causal agent of maize and rice foot rot diseases, but recently it was also found to infect banana and cause severe losses in China. Strains from different sources showed significant diversity in nature, implying complicated evolution history and pathogenic mechanisms.ResultsD. zeae strains were isolated from soft rot banana plants and ornamental monocotyledonous Clivia miniata. Compared with D. zeae strain EC1 isolated from rice, clivia isolates did not show any antimicrobial activity, produced less extracellular enzymes, had a much narrow host ranges, but released higher amount of extracellular polysaccharides (EPS). In contrast, the banana isolates in general produced more extracellular enzymes and EPS than strain EC1. Furthermore, we provided evidence that the banana D. zeae isolate MS2 produces a new antibiotic/phytotoxin(s), which differs from the zeamine toxins produced by rice pathogen D. zeae strain EC1 genetically and in its antimicrobial potency.ConclusionsThe findings from this study expanded the natural host range of D. zeae and highlighted the genetic and phenotypic divergence of D. zeae strains. Conclusions can be drawn from a series of tests that at least two types of D. zeae strains could cause the soft rot disease of banana, with one producing antimicrobial compound while the other producing none, and the D. zeae clivia strains could only infect monocot hosts. D. zeae strains isolated from different sources have diverse virulence characteristics.
| S-EPMC6194671 | biostudies-literature
Project description:Dickeya zeae is a causal agent of rice root rot disease. The pathogen is known to produce a range of virulence factors, including phytotoxic zeamines and extracellular enzymes, but the mechanisms of virulence regulation remain vague. In this study, we identified a SlyA/MarR family transcription factor SlyA in D. zeae strain EC1. Disruption of slyA significantly decreased zeamine production, enhanced swimming and swarming motility, reduced biofilm formation and significantly decreased pathogenicity on rice. Quantitative polymerase chain reaction (qPCR) analysis confirmed the role of SlyA in transcriptional modulation of a range of genes associated with bacterial virulence. In trans expression of slyA in expI mutants recovered the phenotypes of motility and biofilm formation, suggesting that SlyA is downstream of the acylhomoserine lactone-mediated quorum sensing pathway. Taken together, the findings from this study unveil a key transcriptional regulatory factor involved in the modulation of virulence factor production and overall pathogenicity of D. zeae EC1.
| S-EPMC6638372 | biostudies-literature
Project description:Dickeya zeae is the causal agent of rice foot rot disease. The pathogen is known to rely on a range of virulence factors, including phytotoxin zeamines, extracellular enzymes, cell motility, and biofilm, which collectively contribute to the establishment of infections. Phytotoxin zeamines play a critical role in bacterial virulence; signalling pathways and regulatory mechanisms that govern bacterial virulence remain unclear. In this study, we identified a transcriptional regulator OhrR (organic hydroperoxide reductase regulator) that is involved in the regulation of zeamine production in D. zeae EC1. The OhrR null mutant was significantly attenuated in its virulence against rice seed, potato tubers and radish roots. Phenotype analysis showed that OhrR was also involved in the regulation of other virulence traits, including the production of extracellular cellulase, biofilm formation, and swimming/swarming motility. DNA electrophoretic mobility shift assay showed that OhrR directly regulates the transcription of key virulence genes and genes encoding bis-(3'-5')-cyclic dimeric guanosine monophosphate synthetases. Furthermore, OhrR positively regulates the transcription of regulatory genes slyA and fis through binding to their promoter regions. Our findings identify a key regulator of the virulence of D. zeae and add new insights into the complex regulatory network that modulates the physiology and virulence of D. zeae.
| S-EPMC8659590 | biostudies-literature
Project description:Soft rot caused by Dickeya zeae is an important bacterial disease affecting rice and other plants worldwide. In this study, Nanopore and Illumina sequencing platforms were used to sequence the high-quality complete genome of a novel D. zeae strain WH1 (size: 4.68 Mb; depth: 322.37x for Nanopore, 243.51x for Illumina; GC content: 53.59%), which was isolated from healthy rice root surface together with Paenibacillus polymyxa, a potential biocontrol bacterium against D. zeae strain WH1. However, the pure WH1 culture presented severe pathogenicity. Multilocus sequence analysis (MLSA) indicated that strains WH1, EC1, and EC2 isolated from rice were grouped into a clade differentiated from other D. zeae strains. The average nucleotide identity (ANI) and DNA-DNA hybridization (DDH) analyses demonstrated that WH1 was phylogenetically closest to EC2. Furthermore, the pathogenicity determinants and virulence factors of WH1 were mainly analyzed through genomic comparison with complete genomes of other D. zeae strains with high virulence (EC1, EC2, MS1, and MS2). The results revealed that plant cell wall-degrading extracellular enzymes (PCWDEs), flagellar and chemotaxis, and quorum sensing were highly conserved in all analyzed genomes, which were confirmed through phenotypic assays. Besides, WH1 harbored type I, II, III, and VI secretion systems (T1SS, T2SS, T3SS, and T6SS), but lost T4SS and T5SS. Like strains MS1 and MS2 isolated from bananas, WH1 harbored genes encoding both capsule polysaccharide (CPS) and exopolysaccharide (EPS) biosynthesis. The results of pathogenicity assays demonstrated that WH1 produced severe soft rot symptoms on potato tubers, carrots, radishes, and Chinese cabbage. Meanwhile, WH1 also produced phytotoxin(s) to inhibit rice seed germination with an 87% inhibitory rate in laboratory conditions. More importantly, we confirmed that phytotoxin(s) produced by WH1 are different from zeamines produced by EC1. Comparative genomics analyses and phenotypic and pathogenicity assays suggested that WH1 likely evolved through a pathway different from the other D. zeae strains from rice, producing a new type of rice foot rot pathogen. These findings highlight the emergence of a new type of D. zeae strain with high virulence, causing soft rot in rice and other plants.
| S-EPMC9650423 | biostudies-literature
Project description:We report a draft genome sequence of Dickeya zeae strain MS1, which is the causative agent of banana soft rot in China, and we show several of its specific properties compared with those of other D. zeae strains. Genome sequencing provides a tool for understanding the genomic determination of the pathogenicity and phylogeny placement of this pathogen.
| S-EPMC3707573 | biostudies-literature
Project description:Bacteria use signal transduction systems to sense and respond to their external environment. The two-component system CpxA/CpxR senses misfolded envelope protein stress and responds by up-regulating envelope protein factors and down-regulating virulence factors in several animal pathogens. Dickeya dadantii is a phytopathogen equipped with a type III secretion system (T3SS) for manipulating the host immune response. We found that deletion of cpxR enhanced the expression of the T3SS marker gene hrpA in a designated T3SS-inducing minimal medium (MM). In the ∆cpxR mutant, multiple T3SS and c-di-GMP regulators were also up-regulated. Subsequent analysis revealed that deletion of the phosphodiesterase gene egcpB in ∆cpxR abolished the enhanced T3SS expression. This suggested that CpxR suppresses EGcpB levels, causing low T3SS expression in MM. Furthermore, we found that the ∆cpxR mutant displayed low c-di-GMP phenotypes in biofilm formation and swimming. Increased production of cellular c-di-GMP by in trans expression of the diguanylate cyclase gene gcpA was negated in the ∆cpxR mutant. Here, we propose that CpxA/CpxR regulates T3SS expression by manipulating the c-di-GMP network, in turn modifying the multiple physiological activities involved in the response to environmental stresses in D. dadantii.
| S-EPMC9276944 | biostudies-literature